Foraging Modes of Chinstrap Penguins: Contrasts Between Day and Night

Home , Aethia, Argentine Antarctica, Chinstrap penguin, Hop Island, Manx shearwater

MARINE ECOLOGY PROGRESS SERIES Vol. 165: 161-172,1998 Published May 7 Mar Ecol Prog Ser l

Foraging modes of chinstrap penguins: contrasts between day and night

John K. Jansen*, Peter L. Boveng, John L. Bengtson

National Marine Mammal Laboratory, Alaska Fisheries Science Center. National Oceanic and Atmospheric Administration, 7600 Sand Point Way N.E., Building 4, Seattle. Washington 98115-0070, USA

ABSTRACT: Penguins rely on vision to travel and hunt at sea. Vision in marine predators, particularly those hunting phototactic prey under a broad range of light intensities, must be better understood to realize how these species respond to changes in their environment. We studied the effects of daily cycles in light intensity on visual predators by examining the duration and timing of chinstrap penguins' PjrgosceUs antarctica foraging trips and the size, composition, and timing of their meals. We used radio telemetry and stomach-contents sampling to study adult penguins that were provisioning chicks during the summers of 1993 and 1994 at Seal Island, Antarctica. The penguins rarely initiated or terminated foraging trips at night, but otherwise varied the timing and duration of trips to sea. Cluster analyses using departure and arrival times revealed 5 distinct modes of foraging: 3 were strictly diurnal (early, mid-, and late) and 2 were partly nocturnal (overnight and extended). Durations of diurnal trips (4 to 11 h) were shorter than overnight (13 to 14 h) and extended trips (18 to 22 h). Early and rnid- diurnal trips and extended trips were significantly shorter in 1993 than in 1994; late diurnal and overnight trip durations did not differ between years. Diurnal foraging was most common in 1993, whereas overnight foraging predominated in 1994. Shortened diurnal foraging in 1993 appears to have increased the frequency of diurnal foraging by allowing more parent birds to alternate diurnal trips within a single day and by reducing the incidence of birds extending diurnal foraging through the night. That penguins foraged more frequently by day when permitted by shorter trip durations (in 1993) suggests that they opted to forage diurnally whenever possible. Returning dlurnal and overnight foragers had greater than 99 and 74 % Antarctic krill Euphausia superba by weight in their stomachs, respectively However, overnight foragers also returned with significant amounts of highly digested remains of pelagic fish, suggesting birds were in offshore waters talung fish during the night. In contrast, only 1 out of 40 diurnal foragers from both years combined had evidence of fish. Thus, the daily light cycle affected both the timing and duration of chinstrap penguin foraging as well as the type of prey consumed during trips to sea.

KEY WORDS: Die1 activity patterns . Diet composition . Foraging trip duration Myctophid fish . Ecological monitoring . Pygoscelis antarctica . Euphausia superba

INTRODUCTION tin 1990b). Although most seabirds occupy nesting colonies at night, some occasionally or regularly Empirical and experimental evidence points to vision remain at sea (albatrosses: Weimerskirch & Wilson as the primary sense used by birds to negotiate their 1992; storm-petrels: Grubb 1974; shearwaters: Brooke environment by day and night (reviewed by Martin 1990; penguins: Kooyman et al. 1992). Diving seabirds 1990a, b), even though olfactory and magnetic cues regularly experience less light than surface feeders have also proven important (Presti 1985, Verheyden & and there is little evidence that they possess unusual Jouventin 1994, Nevitt et al. 1995). The vast majority of visual capacities (Martin & Young 1984, but see Bow- the world's bird species are active primarily during the maker & Martin 1985). That visual acuity in submarine day, and less than 1 % are active entirely at night (Mar- hunters changes as a function of solar elevation and prey depth has important implications for understand- ing the constraints on foraging behavior in penguins. Antarctic penguins are particularly relevant to under-

O Inter-Research 1998 Resale of full article not permitted Mar Ecol Prog Ser 165: 161-172. 1998

standing visual constraints because most occupy an ing their diet, we were able to compare chinstrap pen- environment characterized by broad ranges of daily guins foraging under different light regimes and deter- light intensities, as well as extreme shifts in daylength. mine whether there may be energetic consequences of Foraging activity in many specles of penguins has varying light intensity. As part of a long-term study of been l~nkedto the daily light cycle. The typical pattern chinstrap penguins and their prey, the goals here were is for most birds to be at sea midday and ashore at 2-fold: to understand the basic foraging patterns of a night (Adelie penguins Pygoscelis adeliae, Yeates marine predator in relation to a fundamental physical 1971; gentoo penguins P. papua and chinstrap pen- variable, light, and to build upon a framework from guins P. antarctica, Trivelpiece et al. 1986; African pen- which future studies will be better able to distinguish guins Spheniscus demersus, Wilson 1985; emperor predator behavior caused by changes in marine prey penguins Aptenodytes forsteri, Kirkwood & Robertson resources from that due to phylogenetic constraints, 1997; Humboldt penguins S. humboldti, Wilson & Wil- such as visual limitations. son 1990; Magellanic penguins S. magellanicus, Sco- laro & Suburo 1994; rockhopper penguins Eudyptes chrysocome, Wilson et al. 1997). Some species, how- METHODS ever, dive at night (macaroni penguins E. chrysolophus, Croxall et al. 1988; king penguins A. patagoni- We studied chinstrap penguins at Seal Island, South cus, Kooyman et al. 1992), despite recent evidence Shetland Islands, Antarctica (60" 59'S, 55" 23' W; Fig. 1) suggesting that when foraging nocturnally, penguins during the austral summers of 1993 and 1994 at 2 have lower prey capture rates than when feeding dur- breeding colonies: North Cove, a colony of approxi- ing the day (Wilson et al. 1993, Piitz & Bost 1994, Wil- mately 900 nests located at the edge of a large inter- son 1995. Wilson & Wilson 1995). A recent model of tidal pool about 70 m from the open sea, and Colony aquiiiic visudi ieeding indicated that daily variations in 72, with approximately 400 nests located on a 300 m light intensity, and thus visual range, may be more long beach (Fig. 1, inset). important to predator feeding than typical variations in Foraging activity. The presence or absence of adult prey abundance (Aksnes & Giske 1993). chinstrap penguins provisioning chicks at North Cove Marked light-dependent rhythms in penguin forag- colony was recorded using radio telemetry from 9 to 22 ing activity (see Wilson et al. 1989, Williams & Rothery January 1993 and from 8 to 19 January 1994. The end 1990, Golombek et al. 1991) suggest that the timing of date in both years was determined by the beginning of trips to sea is an important factor in foraging success. the post-guard phase, the point at which parents leave The synchronization of a colony's foraging patterns in chicks unattended in the colony and are able to forage response to environmental cues may enhance prey independently. Radio transmitters (Advanced Teleme- searching and capture through communication about try Systems, Isanti, MN, USA; reference to trade name feeding conditions (Ward & Zahavi 1973, Brown 1986) does not imply endorsement by National Marine Fish- and group foraging, a widespread behavior in pen- eries Service, NOAA) were deployed on the departing guins (Ainley 1972, Broni 1985, Wilson et al. 1986a, adult from each of 80 nests (1993, n = 40; 1994, n = 40) Norman & Ward 1993). Despite evidence that changes after a nest relief had occurred so as to minimize dis- in light affect the timing and efficiency of penguin for- turbance of the mate on the nest. The foraging activity aging, remarkably few studies have shown more than of instrumented penguins was measured beginning 1 d gross trends in the activity of penguin rookeries in after all 40 penguins were fitted with transmitters; this relation to light cycles (Wilson et al. 1989, Williams & delay was an effort to reduce the effects that handling Rothery 1990). Nor has mu.ch research focused on the the birds and disturbing the colony may have had on potential constraints of variable light for visually-hunt- foraging behavior. Radio transmitters (1.35 cm diame- ing penguins whose daily foraging budget may ter, 6.8 cm length) were attached with epoxy and a include nocturnality at sea. plastic cable tie to feathers at the middle of each pen- In this study, we examined the timing and duration guin's back, posterior to the point of the bird's maxi- of foraging trips taken by chinstrap penguins at mum girth to minimize drag (Bannasch et al. 1994), colonies where adults are known to spend time at sea with the whip antenna trailing behind. The instru- overnight (Bengtson et al. 1993). Because penguins ments were wedge-shaped at the an.terior end, had a relying on vision may be less effective hunters at night, frontal cross-sectional area of 1.4 cm2 and a 28.5 cm we predicted that the birds could enhance foraging by antenna, and weighed 20 g. Attachment of this type of feeding diurnally whenever possible or by adopting transmitter (

Fig. 1 Location of Seal Island within the Antarctic Pemn- suIa region. The dotted line indicates the 1000 m isobath. Inset shows the loca- tions of North Cove colony and Colony 72 in relation to other chinstrap penguin colonies on Seal Island would have energetic and possibly behavioral conse- which were always egested first. During 1993, birds quences (Wilson et al. 1986b, Culik et al. 1994). were lavaged 4 times unless clear water was recovered The timing of departures from and arrivals to the in fewer repetitions. In 1994, birds were always island were monitored by an automated receiving sys- lavaged 4 times; we discovered that even though birds ten1 (Advanced Telemetry Systems) that sampled and may have seemed empty after a second or third lavage, recorded the presence or absence of each radio-tagged additional food could sometimes be extracted subse- bird during a l0 s interval every 15 min. Departure and quently. This procedure provided greater uniformity in arrival times were used to determine foraging trip lavaging and reduced bias in recovering hard parts durations, which were defined as the actual time spent that could be present at the bottom of the stomach and in the water; due to the island's topography, penguins therefore more difficult to extract. Material recovered nesting at North Cove entered and exited the water in in the fourth lavage was always slight and we judged the immediate vicinity of the receiver. All arrival and that any gains obtained from additional lavages would departure times were converted into local apparent not justify further disturbance to the bird. Five birds in times (i.e. 12:OO h occurs at the sun's zenith). Foraging 1993, all arriving in the evening, appeared to have activity patterns determined for a particular date empty stomachs and were lavaged only 3 times. One included only those trips initiated on that day. Obser- bird in 1994 showed signs of distress and was released vations confirmed that all nests included in the sample after the third lavage. had at least 1 chick during the study period in each Stomach samples were collected from 5 different year. Previous analyses indicated that there were no birds every 5-day period throughout chick provision- differences in foraging trip duration between penguins ing (1993, 6 January to 3 February, n = 35; 1994, 8 Jan- rearing 1 versus 2 chicks (Meyer et al. 1997). uary to 12 February, n = 40). Birds were sampled as Food load sizes and diet composition. Diet composi- they arrived in the morning (07:OO to 09:OO h; 1993, n = tion and the mass of food brought ashore were deter- 15; 1994, n = 20) or in the evening (17:OO to 19:OO h; mined by extracting stomach contents from non-instru- 1993, n = 20; 1994, n = 20), alternating between 5-day mented penguins at Colony 72 using a lavage periods. Samples were drained, weighed, sorted into technique (Wilson 1984). Birds that had just completed primary prey categories (i.e. crustaceans, fish, and a foraging trip were captured after they reunited with squid), and then reweighed to determine percent com- their mates at the nest but before feeding their position. Because samples in 1994 were sorted before chick(s). In 1993, each bird's sample was collected in a weighing, more water may have drained out during single bucket, whereas in 1994, the digested portion sorting, possibly biasing these samples toward slightly (i.e. individual prey in pieces) was collected in a sepa- lighter masses compared with 1993. Soft parts, consist- rate bucket from the mostly intact stomach contents, ing primarily of euphausiid krill and fish, were pre- 164 Mar Ecol. Prog Ser 165: 161-172, 1998

served in a 10% formalin solution and stored for subsequent analyses of size, sex, and reproductive status. Hard parts, consisting of fish otoliths and squid beaks, were stored in isopropyl alcohol, dried, and later enu- merated and identified to species. Prey parts were assumed to derive from the most recent foraging trip, an assumption supported by the results (see below). Statistical procedures. Two phases of cluster analyses were used to identify patterns in the timing of departures from and arrivals to the island. First, agglomerative hierarchical clustering, which combined foraging trips into clusters that were then pro- gressively combined with other similar clusters, was used to calculate a coefficient of heterogeneity (Ward's method, SPSS Inc. 1993, Hair et al. 1992). A sharp increase in this coefficient indicated that clusters combined subsequently were of distinctly different departure and/or arrival times. This initial procedure allowed determining the number of clusters and the location of each cluster's center, both of which were necessary for the final analysis. Using each cluster's Local apparenttime center as a seed, a non-hierarchical clustering method Fin. 2. PygosceLis antarctica. Frequency distribution of chin- 'fine-tuned' the results by allowing the switching of strap penguins departing from and arriving at North Cove cluster membership through sequential iterations of colony in relation to time of day for 1993 and 1994 (spline the clustering algorithm (parallel-threshold procedure; curves). Dots show the percentage of birds that were at sea within the respective hourly intervals averaged across all 'quick cluster', SPSS Inc. 1993, Hair et al. 1992). days of the study period. Shaded regions indicate periods We compared durations of trips using 2-way analy- when the sun was below the horizon ses of varia.nce (ANOVA) with year and trip type as the categorical variables. Count data on the frequency of daily foraging patterns and the incidence of fish in 2 clusters representing 2 basic modes of foraging: penguins' diet were analysed using multiway contin- those trips that were initiated and completed within gency tables (i.e. G-test). In these analyses, means and the same day (i.e.were entirely diurnal) and those that count data for each penguin's trip durations and/or were terminated the day following departure (i.e. were daily patterns were not necessarily independent. How- at least partially nocturnal). Multimodal frequency his- ever, because the null hypotheses were extremely tograms of departure time for both diurnal (trimodal) improbable (i.e. 10-3 < p < lO-'), reducing the degrees and overnight (bimodal) clusters in 1993 and 1994 indi- of freedom to levels commensurate with the number of cated these modes were composed of additional forag- birds for any significant test did not increase p beyond ing patterns that required further differentiation (see the 0.05 level. When individual birds were included Schreer & Testa 1995). Plots of arrival time appeared more than once in a sample, summary statistics (i.e. unimodal and therefore were not useful in discriminat- trip duration and percent frequency of daily foraging ing diurnal and overnight sub-groups. After partition- patterns) were calculated using the means from each ing all modes hierarchically, the resulting cluster cen- individual bird. ters (i.e. 3 during the day, 2 overnight) seeded the final nonhierarchical cluster analysis which produced 5 distinct patterns of foraging for both 1993 and 1994 RESULTS (Fig. 3). The timing and durations of the 5 derived trip types for each year, defined as early diurnal (D,), mid- Characteristics of foraging trips diurnal (D,), late diurnal (D,), overnight (ON), and extended (EX),are summarized in Fig. 4. During chick-brooding in 1993 and 1994, the fre- In both years, birds rarely traveled to and from the quency distributions of arrival and departure times of island during the hours of darkness (Figs. 2 & 3). Early radio-tagged chinstrap penguins were approximately diurnal foragers began departing just prior to sunrise, bimodal (Fig. 2). The hierarchical cluster analyses of followed about 1 to 2 h later by mid-diurnal foragers. both years' data, using the timing of departures and Late diurnal foragers began departing about 6 h later arrivals as variables, confirmed the presence of at least on trips which terminated just before sunset. The first Jansen et al.: Foraging modes of penguins 165

penguins to depart on overnight trips (i.e. extended trips) did so amidst the morning diurnal-trip departures. The modal departure time of overnight foragers was during the early evening before sunset. Early morning overlap of different trip types (i.e. D,, ON and EX) resulted in peak percentages of birds at sea at 03:OO to 05:OO h, whereas overlapping nest exchanges at 07:OO to 09:OO h and 14:00 to 17:OO h corresponded to the minimum proportion of birds at sea (Fig. 2). Eighty percent of late diurnal foraging trips represented penguins' first trip of the day and the remaining represented second trips of the day. Most penguins in the former category postponed foraging because they were presumably waiting to be relieved by mates that had embarked on earlier diurnal tnps. Early and late diurnal foragers were apparently those birds from nests where mates alternated diurnal trips on a given day. In these instances, both mates subsequently remained ashore through the night, or the mate that foraged first then departed on its second trip of the day which spanned overnight. Virtually all birds (93 to 99%) that departed in the evening on overnight trips had not foraged previously that day. Differences in trip duration between years depended Departuretime (local apparent) on the type of trip in question (year by trip-type interaction, F4,290= 4.2, p = 3 X w4).Multiple comparisons Fig. 3. Pygosceljs antarctica. Individual foraging trips by using the Tukey HSD procedure indicated that early departure and arrival time for 1993 and 1994. Each aggrega- and mid-diurnal foraging trips were significantly tion of different symbols signifies distinct clusters of either X D,, diurnal (D,, early diurnal; D,, mid-diurnal; D,, late diurnal) or shorter in 1993 than in 1994 (Fig. 4; D,, p = 2 10-4; overnight (ON, overnight; EX, extended) foraging trips (see p = 3 X 10-~),but that late diurnal trips did not differ symbol legend). Shading on the time axes indicates periods statistically between years (p = 0.55). Extended trips when the sun was below the horizon. Dotted lines separate were also shorter in 1993 compared with 1994 (p = 8 X trips completed In one day (lower) from those not completed 10-6), but overnight foraging tnps were not different unhl the following day (upper) in each year (p = 0.87).

Fig. 4. Pygoscelis antarctica. Timing and duration of diurnal (D,, early diurnal; D,,, md-diurnal; D,,late diurnal) and overn~ght foraging trips (ON, overnight; EX, extended) for 1993 and 1994. Numbers in bars indicate mean duration of trip; standard deviation in parentheses. Arrival and departure times and trip durations were averaged across individual-bird means for each trip type. Numbers of trips and penguins exhibiting specific trips are shown in the right-hand columns. Shading indicates periods when the sun was below the horizon. Asterisks next to bars in 1993 denote trip types 12h 18h 0h that were significantly (p < 0.05) shorter than in 1994 Time of day (local apparent) 166 Mar Ecol Prog Ser 165: 161-172, 1998

Table 1. Pygoscelis antarctica. Percent frequency of occurrence of daily foraging patterns (D, = early diurnal, D, = mid-diurnal, D,= late diurnal, ON = overnight. EX = extended, 2D = 2-diurnal, D-ON = 1 diurnaYl overnight, NT = no trip initiated) of chinstrap penguins during chick-brood~ng.Bird-days represent the total number of days on which individual birds were monitored (e.g. 40 birds each belng monitored over a period of 14 d = 560 bird-days)

Year n Daily foraging activity patterns (%) Trips per (bird-days) bird-day Diurnal Overnight Multiple tripsa NT D, Dm DI M ON EX All 2D D-ON

1993 560 9 32 6 47 32 2 34 2 7 10 1.OO 1994 468 8 23 3 34 41 12 53

both years, at least 70% of birds' first of 2 trips on a given day were early diurnal trips

Daily foraging patterns Diet of diurnal and overnight foragers

Chinstrap penguins initiated 0, 1, or 2 foraging trips In 1993 and 1994, all chinstrap penguins returning in on any given day, but the relative frequency of the dif- the morning (i.e. overnight trips) and evening (i.e. ferent patterns differed between the 2 years of this diurnal trips) had predominantly Antarctic krill in their study (Table 1: likelihood ratio test: G = 92.3; p < lO-'; stomachs (Table 2). Fish was more likely to occur in the df = 5; n = 1028 bird-days). A single diurnal trip was stomachs of overnight than diurnal foragers (G = 45.6, most common in 1993, whereas overnight trips pre- df = 1, p i 10-7):fish remains were found almost exclu- dominated in 1994. Extended trips were about 6 times sively in birds that had been feeding overnight (e.g. more common in 1994 than in 1993 (2 vs 12% of bird- only 1 diurnal sample in 1994 had evidence of fish). days). Although it was uncommon for a bird to initiate The predominance of fish in overnight versus diurnal 2 trips in a day, this pattern was considerably more fre- foragers did not change between years (type-of-for- quent in 1993 than 1994, contributing to an overall ager by year interaction: G = 0.20, df = 1, p = 0.65). Fish higher trip frequency in 1993 (Table 1). Birds that initi- occurred more frequently in the samples during 1994 ated 2 trips in one day did so either by taking 2 diurnal than in 1993 (G = 4.12, df = 1, p < 0.05) and were also trips (i.e. early and late diurnal trips) or by combining 1 more abundant numerically (comparison of number of early diurnal with 1 overnight foraging trip. Birds com- otoliths between years: t = 1.97, df = 23, p = 0.035, pleting 2 diurnal trips departed on the second trip Table 2). Remnants of squid and amphipods were within about 3 h of terminating the first, probably not observed only rarely, composing

Table 2. Pyyoscelis antarctica. Diet mass and composition and frequency of occurrence of fish in the diet of chinstrap penguins sampled after returning from diurnal (D) and overnight (ON) foraging trips. Intact and digested portions of the diet samples were examined separately in 1994 only. na: not applicable; t: trace, i.e. no flesh was recovered, only otoliths and eye lenses were found (weight < 1 %). Unidentifiable prey rounds out any remaining proportions of diet composition by weight

Year Type of n Mean % lntact % composition by weight % of samples No. of forager weight (by wt) - Intact a Digested- with evidence otoliths (S) (SDI Krill Fish Squid Krill Fish Squid of fish Meanb Range 1993 D 20 356 (146) na 100 - - na na na 0 - - ON 15 407 (148) na 96 4' - na na na 53 11 5-33 1994 D 20 595 (207) 6 2 100 t 98 t - 5 6 na ON 20 499 (140) 60 96 3 - 42 43

cates that flsh remains are not retained in the stomach from the island. It is noteworthy that regardless of the from one trip to the end of the next. behavioral context in which darkness occurs (e.g. Fish recovered from overnight foragers were never active at sea or relatively inactive at the nest) the same intact and usually occurred in the form of bones, reluctance to transit to/from the island is observed. otoliths, and small pieces of flesh. In both years, the Because penguins are active at sea during the night, fish prey of overnight foragers were primarily mycto- their reluctance to attempt a landing is presumably not phids (95%), such as Electrons antarctica, E. carls- governed strictly by a light-mediated endogenous bergi, Gymnoscopelus nicholsi, and Krefftichthys clock (see Cockrem 1990).This avoidance may instead anderssoni and less commonly (5 %) the paralepidid reflect an underlying behavioral adaptation to other Notolepis coatsi. During lavaging, pieces of fish ap- environmental constraints, such as risk of predation or peared only after fresher krill had been regurgitated. lack of prominent visual cues for navigation. The appearance of fish usually indicated food had Leopard seals Hydrurga leptonyx hunt penguins at come from the bottom of the stomach as subsequent Seal Island (authors' pers. obs.) and may influence the lavaging produced little additional prey. It was appar- number of trips taken by adults provisioning chicks ent any mixing that may have occurred in the stomach (Chappell et al. 1993).Chappell et al. (1993), who esti- during lavaging was not sufficient to obscure the strat- mated that 11% of breeding Adelie penguins at ification of prey in the gut. Whereas in 1993 only 1 Palmer Station were eaten annually by leopard seals, sample from an overnight forager contained parts of calculated the risk of Adelie mortality by predation at fish flesh large enough to be recovered (286 g), 15 0.4 % per trip, a substantial risk when integrated over samples in 1994 contained between 2 and 347 g of fish the breeding season. The impact of leopard seal pre- flesh. Fish composed at least one-half of the identifi- dation on breeding penguin populations elsewhere able prey (by weight) in the digested samples from was deemed minimal (e.g. 2.4 % per annum, Miiller- overnight foragers in 1994 (Table 2). Schwarze 1984; 2.7 %, Rogers & Bryden 1995) or incon- The timing of foraging trips (diurnal vs nocturnal) sequential (e.g. 2 kills per 13000 birds observed in had no significant effect on the mass of food brought 120 h over 20 d at 3 rookeries, Hofman et al. 1974; ashore in either year (2-way ANCOVA with day of the 0 kills per 50000 birds over 21 d, Muller-Schwarze & year as the covariate: F,,,, = 0.186, p = 0.67). However, Muller-Schwarze 1975). the mean weight of samples was heavier in 1994 than The timing of leopard seal predation on penguins in 1993 (F,,,, = 15.61, p i 0.001). The increased food also appears variable between sites, although detailed mass in 1994 may have been the result of larger food information on diel patterns in hunting behavior is loads in diurnal than in overnight foragers, but the sparse. Observations at several penguin breeding sites trend was not quite significant (year by trip-type inter- are difficult to interpret. Different studies have con- action, F1,,,= 2.86, p = 0.09). cluded that leopard seals exhibit no diel rhythm in hunting behavior (Cape Crozier, Penney & Lowry 1967); are primarily in the water at night (Ross Island, DISCUSSION Miiller-Schwarze 1971); haul out midday (Palmer Sta- tion, Hofman et al. 1974); or capture penguins only Arrivals and departures at night during the day and haul out during the night (Elephant Island, Conroy et al. 1975). At Seal Island, leopard Occasional nocturnality in otherwise diurnal birds is seals were observed consuming penguins during the relatively common (Martin 1990a), but how these birds day primarily at Beaker Bay (Fig. 1; Lisa M. Hiruki, cope with the constraints of darkness is not well National Marine Mammal Laboratory, Seattle, WA, known. The restricted lifestyle imposed on truly noc- USA, unpubl. data), an area transited by as many as turnal birds (Martin 1986) suggests that a high degree 14000 birds daily (i.e. 28000 l-way transits). Only 4 of of specialization is required to persist in a low-light en- 42 penguin captures observed during 1987-1995 vironment. Still, birds that are primarily diurnal com- occurred at North Cove, which encompasses coastline monly travel long distances at night, albeit by flying at transited by fewer than 5000 birds per day. A distinct altitudes well away from obstacles (Martin 1990b). peak in observed predation (i.e. between 08:OO and Chinstrap penguins at Seal Island, although known to 21:OO h) occurred at -17:OO h which corresponds dive during nocturnal excursions to sea (Bengtson et closely to the evening peak in birds transiting the coast al. 1993), apparently lack the ability or motivation to (Fig. 2). Penguins at Seal Island may avoid the coast- transit the coastline during the darkest hours of the line at night in part because of an increased predatory night. The paucity of arrivals to and departures from threat, but the variable nature of leopard seal behavior North Cove between 22:OO and 02:OO h suggests that and impacts - even though penguins show distinct light intensity restricts the timing of movements to and foraging activity patterns (see references above) - 168 Mar Ecol Prog SE

suggests that more predictable factors may constraln Among birds at sea, increasing light intensity may their behavior. trigger continued foraging. Because birds returned A constraint on penguin orientation in an environ- from overnight trips about 3 h later than birds depart- ment with few visual cues may restrict nocturnal ing at sunrise, it is clear that birds were not simply movements to and from Seal Island. Unobscured sun- waiting offshore for light intensity to increase before light was necessary for Adelie penguins to navigate attempting to land. Changes in light intensity also accurately to the ice edge in the Ross Sea (Emlen & elicit vertical migrations in krill swarms. Antarctic eu- Penney 1966), even though the use of magnetic fields phausiids sink and form dense concentrations during by birds to navigate is also generally accepted the day and rise to the surface and disperse at night (reviewed by Presti 1985 and Moore 1987). Consider- (Kalinowski & Witek 1980, Everson 1982, Everson & able evidence, however, indicates that visual cues are Murphy 1987, Ringelberg 1995), although die1 patterns equally or more important than magnetic fields for in krill depth and density have not always been ob- initiating and maintaining a course in birds migrating served (Miller & Hampton 1989). Even though krill by day and night (Martin 1990b and references become less available to diving predators as they grad- therein). Further, reduced light is likely to impose lim- ually descend at sunrise, rapidly increasing light inten- itations on the ability of penguins to negotiate the sity may provide a narrow 'window' when visual hunt- complex and potent~ally hazardous coastline of Seal ing could actually be enhanced. In both years, the daily Island (i.e. heavy surf along rocky bluffs and shore- peak in proportion of birds at sea occurred just after line). That some commuting penguins are injured sunrise (Fig. 2). Termination of continuous nest atten- during periods of intense surf, even during daylight dance during the post-guard phase in chinstrap pen- (authors' pers, obs.), confirms there are risks associ- guins at Seal Island coincided with a shift to diurnal ated with crossing the intertidal zone. If visual acuity foraging with peak departures occurring at or before in penguins is reduced at night, it could further limit sunrise (Jansen 1996). Moreover, penguin studies that their ability to transit the shoreline safely. Spatial res- examined the actual timing of prey capture during olution in birds at low light levels is unknown (except overnight trips (Wilson 1995) or trips longer than 3 d for one species of owl; Fite 1973). On theoretical (Wilson et al. 1993, Piitz & Bost 1994) indicated en- grounds, however, it is understood that the vertebrate hanced foraging effort and success at dawn and dusk. eye is incapab1.e of a high degree of spatial resolution The durations of foraging trips on a particular day at the lowest environmental light intensities (Snyder affect whether mates predominantly alternate diurnal et al. 1977). Martin (1990b) concluded that birds trips (i.e. both mates spend the night ashore), as may migrating at night, even under maximum moonlight, have occurred in 1993, or alternate diurnal with over- were able to detect only the grossest details of their night foraging, a pattern more apparent in 1994. environment. The light gathering capacity and visual Shorter diurnal foraging trips early in the day in 1993 sensitivity of the penguin eye fall within the range (-8 h) apparently allowed both members of more pairs typically found in mammals and birds (Martin & to forage exclusively during a limited period of day- Young 1984).Thus, we expect that darkness impacts light (-18 h), causing a decrease in overnight foraging. the ability of chinstrap penguins to navigate the near Longer diurnal foraging trips in 1994 (- 11 h) would featureless environment offshore and the precipitous preclude more parents from each completing diurnal wave-battered coastlines commonly encountered near trips within the same daylight period (i.e. second trips colony sites. from such nests occurred later and could not be completed before the 'transit window' closed). That birds foraged more often during the day in 1993, when diur- Timing and frequency of foraging nal trip durations were generally shorter, suggests that birds were selecting the h.ours of daylight for foraging The periodic and synchronized nature of the teleme- whenever possible. In some years, overnight foraging try data suggests that changing light intensity affects could be a favored strategy. The 2 years reported here, chinstrap penguins' foraging trip departures and arri- however, suggest that overnight trips can be the con- vals. Specifically, the close correspondence between sequence of later nest reliefs (i.e, longer trips by the early diurnal departures and sunrise indicates that nest mate). birds that spent the night ashore responded to increas- Similar to penguins at Seal Island, brooding chin- ing morning light; later modes of diurnal foraging indi- strap penguins at nearby Elephant Island (61.2"s) cate that other blrds delayed departures to wait for a exhibited a bimodal pattern of departures (04:OO h and mate's arrival. Relatively synchronous arrivals proba- 12:OO h) and arrivals (10:OO h and 19:OO h) (Conroy et bly reflect the combined effects of changing light al. 1975). Birds that stayed at the nest with their mates intensity and similar trip duratlons by ~ndlviduals. overnight departed just after sunrise, supporting the Jansen et al.: Foragi.ng modes of pengulns 169

role of light as an important controlling factor. How- whether the birds are feeding opportunistically on the ever, the paucity of evening departures (i.e. most nests most available prey species, which changes through were occupied by pairs overnight), coupled with mid- the night, or are shifting their focus from fish to krill, day nest exchanges (see Figs. 3 & 5 in Conroy et al. perhaps by moving inshore. That myctophids appar- 1975), suggests shorter diurnal trips and fewer birds ently are near the surface until morning (Zasel'sliy et foraging overnight at Elephant Island than at Seal al. 1985) suggests the latter. Island. These differences in foraging may have Because myctophid fish are primarily meso-epi- resulted from contrasting prey availability. Enhanced pelagic (Zasel'sliy et al. 1985, Perissinotto & McQuaid prey access could have shortened the typical daily for- 1992), piscivorous, land-breeding predators can only aging cycle at Elephant Island, allowing both mates to meet their daily food requirement by traveling ex- feed diurnally. tended distances to oceanic areas (e.g. king penguins travel 28 to 1489 km offshore; Stahl et al. 1985, Adams & Klages 1987, Kooyman et al. 1992, Jouventin et al. Light-dependent differences in diet 1994). Consistent with this pattern, a recent study tracking chinstrap penguins to their foraging grounds The stark contrast between the fresh krill recovered north of Seal Island showed that birds foraging diur- first and the digested fish and krill recovered last from nally remained close to the island, whereas overnight penguins that foraged overnight indicates fish were foragers traveled to and beyond the edge of the conti- taken early during foraging trips, whereas krill were nental shelf (authors' unpubl. data). For penguins for- taken during feeding periods throughout trips. Free- aging at night, it may be energetically worthwhile to ranging African and captive gentoo penguins are travel far offshore to obtain energy-rich prey (see Obst known to digest fish down to bones and otoliths within et al. 1995) that are relatively easy to capture (note that 10 to 16 h (Wilson et al. 1985, Gales 1987), consistent myctophid photophores may be visible to penguins). with the advanced digestion of fish from chinstrap pen- The least energy-rich myctophid consumed in this guins sampled after overnight trips of 14 h typical study, Gymnoscopelus nicholsi, has 17 and 49% more duration. The abrupt change in the state of digestion energy per unit wet weight than adult gravid female indicated that the switch in prey occurred during a hia- and adult male Antarctic krill, respectively; Electrona tus in feeding. Wilson (1995) observed peaks in prey species represent a 72 to 120% energy gain over krill ingestion around sunrise and sunset, and a pause in (T. Ichii, National Research Institute of Far Seas Fish- feeding at night, by a chinstrap penguin foraging at eries, 5-7-1 Ondo, Shimizu, 424 Japan, unpubl. data; King George Island. It may be that success at feeding specimens collected near Seal Island during summer on myctophids declines through the night, after which 1994/95). Meals obtained overnight were similar in the penguins switch solely to krill, perhaps closer to mass to diurnal meals even though overnight foragers Seal Island, as the morning light increases. Stratifica- spent 30 to 80 % more time in apparently more distant tion was not observed in stomach contents of diurnal feeding areas. However, considering the reconstructed foragers, suggesting they consume krill exclusively mass of the fish and their greater energetic value, and take prey at more regular intervals than those for- overnight foragers at least partly covered the additional aging overnight. These scenarios are consistent with energetic overhead of longer duration, more distant, patterns in the spatial and ten~poral distribution of trips. Chinstrap penguins at Seal Island that forage chinstrap penguin prey. overnight may use distant, but profitable, resources A die1 vertical migration from depths of 150 to 400 m (myctophids) to feed then~selves, but rely on inshore during the day to the upper 100 m at night has been prey (krill) to provision offspring, as suggested for king demonstrated in 2 of the 4 myctophid species (Elec- penguins (Jouventin et al. 1994, Cherel et al. 1996). t~-onacarlsbergj and Krefftichthys anderssoni) taken Even though our findings suggest that myctophids by penguins in this study (Zasel'sliy et al. 1985, are an important source of energy for overnight for- Perissinotto & McQuaid 1992). These upward migra- agers, all fish remains were probably not retained in tions of myctophid fish correspond with periods of the stomach until birds arrived ashore; myctophids are enhanced feeding of fish on krill near the surface at probably eaten at the most distant point of penguins' sunset and just before sunrise (Zasel'sliy et al. 1985, foraging excursions. Experimental feeding trials on Podrazhanskaia & Tarverdieva 1991). Our findings gentoo, little Eudyptula minor, and African penguins support the view that myctophids move to the surface suggest that otoliths can be passed from the stomach at dusk and become more vulnerable to chinstrap pen- within 1 to 4 h after consumption and that 12, 58, and guins from Seal Island. Subsequently, penguins stop loo%, respectively, may be undetected by lavaging feeding on fish-probably during the first half of the after 16 h (Wilson et al. 1985, Gales 1987). The contri- trip-and begin taking krill exclusively. It is unclear bution of fish to penguin energy budgets may be 1.70 Mar Ecol Prog Ser

underestimated, especially in populations where trips that small chicks are continuously attended. The for- to sea exceed the time taken to digest fish (e.g. chin- mer requires the regular acquisition of food and the strap penguins at Signy and King George Islands; Lish- 1.atter restricts the decision about when (and appar- man 1985, Trivelpiece et al. 1990). ently where) to acquire it. Although birds may not Although chinstrap penguins are considered to be prefer evening departures, the regularity of overnight krill specialists (Volkman et al. 1980, Lishman 1985, foraging at Seal Island suggests that these trips are Trivelpiece et al. 1990), the daily timing of foraging has necessary to maintain the timely delivery of food to rarely been considered. For example, chinstrap pen- chicks when a meal might otherwise be missed. Even guins in the vicinity of Elephant Island had 96% though birds have apparently adapted to a nocturnal Euphausia superba in their stomachs (by weight), with habit at sea, penguins avoided transiting the island's few birds (7%) reportedly showing evidence of fish coastline under darkness and foraged more frequently (Croxall & Furse 1980). At 2 particular sites on by day when permitted by shorter diurnal trip dura- Clarence Island, 40% of the birds were reported to tions (of their mates). These findings suggest that have eaten fish, although it is difficult to assess fish darkness could restrict visually-based movement and importance because number of otoliths and sampling feeding. A behavioral adjustment countering the time were not noted (Croxall & Furse 1980). Similarly, apparent costs of nocturnal foraging is for parents to during 6 breeding seasons at Admiralty Bay, King embark on longer, more distant foraging trips to pur- George Island, stomach sampling indicated that chin- sue energy-rich bioluminescjng myctophid fish. strap penguins relied heavily on krill in all years This study demonstrates the need to consider pho- except one (Jablonski 1985, Trivelpiece et al. 1990). In toperiodicity when examining penguin foraging be- 1980/81, sampling conducted by Jablonski (1985) indi- havior. Die1 changes in light intensity apparently com- cated that 65 % of chinstrap diet was composed of fish pel chinstrap penquins to use feeding modes that differ with the remainder being krill (l? %) and amphipods in d~etand duration. These distinct modes reveal com- (5?h). He also showed a greater frequency of fish in the plex interactions between foraging performance, prey diet of 'morning' (l00 %; n = 48) versus 'evening' (46 %; availability, and the physical environment. Because n = 49) foragers, which may have resulted from feeding light intensity affects such fundamental aspects as modes similar to those reported here. At Seal Island in predators' visual range and prey distribution, similarly 1989/90, fish occurred in chinstrap penguins lavaged complex interactions can be expected in other studies before noon 10 times as frequently as those sampled of visual predators and their prey. after noon [79% (n = 14 birds) vs 7 % (n = 26),respectively; authors' unpubl. data]. It is clear that whlle Acknowledgements. We thank members of the fleld teams, chinstrap penguins at Seal Island rely on krill they do including Don Croll, Mike Goebel, Lisa H~ruki,William Meyer, Steve Osmek, Mike Schwartz, and Brian Walker for not specialize on krill exclusively, but rather appear to help in establishing field protocols, enthusiastic data collec- feed on different prey based on temporal and spatial tion, and for many helpful discussions. Many of the ideas pre- availability. The generality of this finding is unknown; sented here were conceived through discussions with the future diet samp1in.g should consider the potential for senior author's (J.K.J.) thesis committee at the Un~versityof Oregon's Institute of Marine Biology, and we especially thank die1 variability in diet composition. Moreover, inter- Jan Hodder for her insightful contributions. We are also grate- preting the importance of a particular prey to chinstrap ful to Jason Baker, Lisa Hiruki, Harriet Huber. Gerald Kooy- penguins through diet sampling requires knowledge man, Robert RusseU. Mike Schwartz and 3 anonymous re- of potential foraging strategies and factors influencing viewers for valuable comments on earller drafts Steve Osmek the relative frequency of those behaviors within and conducted the diet analyses that produced the unpublished results for 1990. Taro Ichii of Japan's National Research Insti- between years. For instance, this study suggests that tute of Far Seas Fisheries helped in identifying fish otoliths. shifts in diurnal trip duration, which could be affected Thanks are also extended to the officers and crew of the by krill availability, can influence the relative occur- NOAA ship 'Surveyor' and the MV 'Explorer' for exceptional rence of f0ragin.g at night, when feeding behavior may log~stical support This research was supported by the Nat~onalOceanic and Atmospheric Adm.inistration, National be redirected toward myctophids. marine Fisheries Service, as part of its Antarctic Marine Liv- ing Resources Program.

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Editorial responsibility: Otto fine (Editor), Submitted: September 25, 1997; Accepted: February 13, 1998 OldendorfILuhe, Germany Proofs received from author(s): April 20, 1998